Management of soilborne diseases of potato
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CSIRO PUBLISHING Keynote Paper
www.publish.csiro.au/journals/app Australasian Plant Pathology, 2007, 36, 109–115
Management of soilborne diseases of potato
N. C. GudmestadA,B , R. J. TaylorA and J. S. PascheA
A
Department of Plant Pathology, North Dakota State University, Fargo, North Dakota 58105, USA.
B
Corresponding author. Email: Neil.Gudmestad@ndsu.edu
Abstract. A large number of soilborne diseases that affect potato are important in the United States. In the Midwestern
USA, early dying, involving Verticillium dahliae and Colletotrichum coccodes and the storage rots, pink rot and leak
tuber rot, caused by Phytophthora erythroseptica and Pythium ultimum are among the most serious. Various aspects of the
biology and aetiology of these pathogens have been investigated to improve our understanding of the factors involved in
disease development. These studies have addressed knowledge gaps and have assisted in the development of management
strategies and tactics for each disease. Disease management integrates cultural practices, use of agrochemicals and to
some degree, host resistance. Unfortunately, cultural management practices alone are currently inadequate to control these
diseases, causing the potato industry to become over-reliant on the use of agrochemicals for effective management. Current
research efforts are directed at the identification and incorporation of genetic resistance into cultivars with acceptable
horticultural characteristics to provide more effective disease management.
Introduction triggers the use of the soil fumigant metam sodium (Nicot and
Several very important potato pathogens in the USA originate Rouse 1987), although more recent work has cast doubt on the
from soilborne inoculum. The most important of these soilborne relationship of V. dahliae soil populations and yield of potato
diseases can be separated into two primary groups; diseases (Davis et al. 2001). This more recent work suggests edaphic
that affect crop development and diseases that affect tuber factors, such as organic matter and sodium concentration in
quality. Soilborne diseases that affect crop development include the soil, influence disease severity, potato yield and perhaps
Rhizoctonia canker, black dot, potato early dying (Verticillium inoculum efficacy.
wilt) and numerous nematodes. Soilborne diseases that affect Although V. dahliae is the most important pathogen in
tuber quality include common scab, powdery scab, pink rot, this complex, the root lesion nematode Pratylenchus penetrans
leak, black dot, black scurf, root knot nematode, and Fusarium and the black dot pathogen Colletotrichum coccodes are
dry rot. Among these, black dot, Verticillium wilt, pink rot and also involved (Otazu et al. 1978; Davis and Huisman 2001).
leak tuber rot are the most important in the Midwestern states Coinfection of V. dahliae and C. coccodes in the same plant
of North Dakota and Minnesota. Disease management includes hastens plant maturity and reduces plant development more so
the integration of crop rotation, cultural practices, host resistance than either pathogen alone (Otazu et al. 1978; Tsror (Lahkim)
and agrochemicals. et al. 1999). Most potato cultivars are very susceptible to
Potato early dying is arguably the most economically V. dahliae and C. coccodes. However, two cultivars, Alturas
damaging disease complex of potato in the USA when and Ranger Russet (Novy et al. 2003), developed within the last
considering direct losses of yield and quality and the cost of decade, have resistance or tolerance to Verticillium wilt. They
control (Rowe and Powelson 2002). In the Midwestern USA, the now account for nearly 10% of potato production for French
disease complex is most important in the French fry processing fry processing. Unfortunately, the rest of this market sector
sector, which relies on long season potato cultivars such as relies on the use of metam sodium as a soil fumigant for the
Russet Burbank. Verticillium dahliae is generally regarded as management of potato early dying. There have been numerous
the primary pathogen involved in this disease complex (Rowe examples of control failure with metam sodium that required
and Powelson 2002). This fungus survives as microsclerotia in investigation, especially since this agrochemical is expensive
the soil for extended periods of time (Davis and Huisman 2001). and can potentially have significant negative impacts on the
V. dahliae is a variable fungus, separated into groups based on environment.
vegetative compatibility (Rowe and Powelson 2002). Vegetative Pink rot and leak tuber rot, collectively referred to as ‘water
compatibility group (VCG) 4 is the most aggressive on potato, rots’, are caused primarily by the soilborne fungi Phytophthora
with subgroup 4A the most important (Joaquim and Rowe 1991; erythroseptica and Pythium ultimum, respectively. These two
Strausbaugh 1993). Soil inoculum levels are known to influence fungi cause problems with tuber quality and integrity of the
disease severity (Ben-Yephet and Szmulewich 1985). Previous stored potato crop. One could argue that in the USA, tuber rots
research in the Midwestern USA has demonstrated that an caused by P. erythroseptica and P. ultimum are economically
economic threshold of ≥8 V. dahliae propagules/g (vppg) of soil more important on a yearly basis than any other disease affecting
© Australasian Plant Pathology Society 2007 10.1071/AP06091 0815-3191/07/020109110 Australasian Plant Pathology N. C. Gudmestad et al.
tuber quality. Late blight tuber rot infections tend to be acute and has demonstrated that tillage practices influence survival of
spectacularly devastating when they occur. However, in most both pathogens as well as the efficacy of metam sodium (Taylor
production years, few growers experience economic loss from et al. 2005).
this phase of the disease. Pink rot and leak tuber rot are chronic Conservation tillage is a commonly used practice in crops
and endemic diseases, present every year in nearly every potato planted in rotation with potato. Conservation tillage, known
production region. Storage rot surveys conducted in each of the variously as reduced tillage, no tillage or minimum tillage,
past nine years in North Dakota and Minnesota indicate that pink are practices intended to preserve crop residue near the soil
rot and leak tuber rot are of almost equal importance with one surface to enhance soil organic matter content, protect soil from
or the other being more important in any one year (R. J. Taylor erosion and several other benefits. Chisel ploughing, as opposed
and N. C. Gudmestad, unpubl. data). to the traditional tillage practice of mouldboard ploughing,
Differences in the aetiology of pink rot and leak tuber rot is the most frequently used method of conservation tillage.
are significant, which ultimately affects disease management Mechanical harvesting of potatoes leaves the crop residue at the
(Taylor et al. 2004). Infection of pink rot usually occurs in soil surface where V. dahliae resides. The equipment currently
the field, before harvest, when zoospores of P. erythroseptica utilised for reduced tillage practices do little to incorporate
infect stolons, tuber eyes or lenticels (Lambert and Salas or mix the soil layers (Taylor et al. 2005), resulting in >70%
2001). Infection by P. ultimum is strictly through wounds of the V. dahliae inoculum residing in the upper 10 cm of
made at harvest (Salas and Secor 2001). Cultural practices soil. In contrast, mouldboard ploughing inverts the soil strata
alone are frequently inadequate to manage pink rot and leak thereby causing a significant amount of the V. dahliae inocula
tuber rot, which has caused the potato industry to become to reside in soil at depths of 20 cm. We feel that older studies,
overly reliant on the use of mefenoxam (metalaxyl)-based and those studies conducted in potato production areas where
fungicides for disease control. Unfortunately, mefenoxam mouldboard ploughing is still common, explain the contrasting
resistance has been reported in P. ultimum and is widespread results between our work and that found in the literature.
in P. erythroseptica (Taylor et al. 2002). Understanding the Since metam sodium is applied as a liquid but must volatilise
impact of mefenoxam resistance on disease management into a gas to permeate through the soil profile to act on the
in addition to the development of alternative and effective microsclerotia of V. dahliae, the concentration of soil inoculum
management strategies is of utmost importance for the control of at the surface provides a significant challenge in successful soil
water rots. fumigation. Our studies concluded that much of the metam
The discussion that follows is intended to demonstrate the sodium gas is lost to the atmosphere in the upper 10 cm resulting
approach our research group has undertaken to more fully in very poor mortality of the V. dahliae microsclerotia and
understand the biology and aetiology of the pathogens involved the concomitant loss of disease control (Taylor et al. 2005).
in the early dying complex and the water rot storage disease Simple inversion of the soil strata using mouldboard ploughing
syndrome. The overall goal has been to fill the knowledge gaps significantly improved disease control of early dying. Not only
for each disease-causing pathogen so as to improve disease does mouldboard ploughing improve the efficacy of metam
management options for the potato industry. Whenever possible, sodium fumigation (Taylor et al. 2005) but this tillage practice
our data will be discussed within the context of the information increases the mortality of V. dahliae propagules in the soil
generated by other research groups where these diseases are also (Fig. 1a) and also significantly reduces black dot (Fig. 1b), an
important. observation that supports previous studies (Denner et al. 2000).
These results are in direct contrast with an earlier study on
Early dying Rhizoctonia solani, in which case disease severity was reduced
Although the biology and ecology of V. dahliae is relatively with conventional tillage practices compared to mouldboard
well understood, there are aspects of the pathogen that required ploughing (Gudmestad et al. 1978).
further definition to improve disease management. Soil The length of rotation also affects the management of early
pathogens can be affected by several soil physical properties dying, primarily by affecting the soil populations of V. dahliae
(Rothrock 1992), and tillage is known to affect several of (Fig. 2). Soil populations of V. dahliae can be 2- to 4-fold
these properties and exert an influence on disease development higher in soils with a 2 year potato rotation (Fig. 2a) compared
(Peters et al. 2003, 2004). With Verticillium spp., soil inoculum to a 3-year potato rotation (one potato crop in three years)
levels are known to vary spatially and temporally, but much (Fig. 2b). Higher soil populations make effective control via
of that work was interpolated and quite old. Wilhelm (1950) soil fumigation with metam sodium much more difficult. For
demonstrated that the vertical distribution of Verticillium albo- example, if we accept an economic threshold of 8 vppg (Nicot
atrum varied considerably, with the greatest proportion residing and Rouse 1987) and an efficacy of metam sodium of no more
in the upper 30 cm of soil, nearest the surface. More recently, than 70% (Taylor et al. 2005), then it is easy to understand that
V. dahliae was found to be concentrated primarily in the upper soil populations of V. dahliae of >25 vppg before fumigation
20 cm soil strata (Ben-Yephet and Szmulewich 1985; Hamm will likely leave a resident population above threshold. For this
et al. 2003). Results of our research in the Midwestern USA reason, our recommendations are that potato rotation durations
has determined that the inocula of V. dahliae is concentrated in should not exceed one potato crop in three years. Additionally,
the upper 10 cm (Taylor et al. 2005). We believe that changes in seasonal variations of V. dahliae populations clearly indicate that
tillage practices, specifically those directed at soil conservation, it takes one and a half to two years before the decomposition of
are directly responsible for the concentration of inoculum in the potato crop debris will be sufficient enough to obtain effective
upper 10 cm soil strata. Research by our potato pathology group fumigation (Joaquim et al. 1988; Taylor et al. 2005). WhenManagement of soilborne diseases of potato Australasian Plant Pathology 111
100 50
(a) (a)
No. of V. dahliae propagules/g
Mouldboard plough a
Conventional tillage
80 40 a
% Reduction
60 30
b b
20 b
40 b
10
20
0
0
3 May 21 May 25 July 7 Aug. 20 Sept. 21 May
Field 1 Field 2
2003
100
(b) 50 (b)
% Black dot disease control
No. of V. dahliae propagules/g
80
40
60 30
40 20
a
20 10 ab
b b
b
b
0 0
Field 1 Field 2 16 May 21 May 25 July 8 Aug. 20 Sept. 21 May
2003
Fig. 1. Effect of mouldboard ploughing relative to conventional tillage on
reduction of Verticillium dahliae microsclerotia in the upper 20 cm of soil Fig. 2. Propagules of Vertillium dahliae recovered over the course of a
(a) and on the control of black dot (b) in two fields in Minnesota. Data taken growing season from field soils planted to potato in a 2-year (a) and 3-year
on a georeferenced basis in two fields split by tillage practice over a 3-year (b) rotation. Soils were sampled in 2002, which was the year before each
period, 2003–2005. field was cropped to potato. (Data taken from Taylor et al. 2005)
V. dahliae soil inoculum is protected by crop debris it cannot compared with soilborne inoculum (Cullen et al. 2002), but
be killed by metam sodium, resulting in poor efficacy (Taylor there is information suggesting the importance of either source
et al. 2005). The data generated by our research group have been may be cultivar specific (Nitzan et al. 2005). Unfortunately,
important in reducing soil populations through cultural practices metam sodium is ineffective in the management of black dot,
such as mouldboard ploughing and by improving efficacy of presumably because the microsclerotia of C. coccodes are
metam sodium applications. significantly larger than those of V. dahliae making them resistant
The early dying complex in the USA is exacerbated by the to this biocide.
presence of C. coccodes – the black dot pathogen. C. coccodes Our research group has concentrated our efforts on
can cause reductions in yield and quality by itself (Johnson understanding the infection frequency of various plant parts
1994; Tsror (Lahkim) et al. 1999), but appears to be particularly relative to yield (Gudmestad et al. 2005). Previous research
important with coinfections of V. dahliae (Otazu et al. 1978; in Europe has suggested that belowground plant parts, stems,
Tsror (Lahkim) and Hazanovsky 2001). A great deal of attention stolons and roots are the most rapidly colonised by C. coccodes
has been given to tuber infections of C. coccodes, which (Read and Hide 1995; Andrivon et al. 1998). Our data
causes a tuber blemish and much of what we know about demonstrate that aboveground stems are more rapidly colonised
the disease black dot is from this very important phase of by this fungus and that yield loss is associated with the infection
the disease (Read and Hide 1995; Lees and Hilton 2003). frequency of this plant part (Fig. 3) (Gudmestad et al. 2005).
However, foliar infections of C. coccodes are known to occur Data obtained to date also suggest that soilborne inoculum of
and to be an important component of the disease (Johnson ≥70 C. coccodes propagules/g of soil is sufficient to negatively
and Miliczky 1993; Johnson 1994). It also appears that the affect tuber yield. We are in the process of developing a
fungus preferentially grows towards the roots and stolons duplex real-time PCR technique to quantify soil populations of
rather than towards the apex (Nitzan et al. 2006b). Whether V. dahliae and C. coccodes (N. C. Gudmestad and J. S. Pasche,
or not this is the mechanism by which the fungus reaches unpubl. data). The C. coccodes primers used in the duplex are
the vascular tissue is not known at this time. We also do based on previously published studies (Cullen et al. 2002) and
not know the importance of seedborne (Johnson et al. 1997) the DNA sequences used to develop the V. dahliae were derived112 Australasian Plant Pathology N. C. Gudmestad et al.
100 44 (a)
90
Aboveground stem y = –1.2334ln(x) + 42.576
42
C. coccodes infection (%)
Belowground stem R2 = 0.844
80
Crossing point
Root 40
70
Stolon
60 38
50 36
40 34
30
32
20
10 30
0 500 1000 1500 2000 2500 3000 3500
0
7 14 21 28 35 42 49 56 63 70 77 84 No. of microsclerotia/g
Days after emergence
120
(b)
Fig. 3. Frequency of Colletotrichum coccodes recovery from aboveground
No. of microsclerotia/g
stems, belowground stems, stolons, roots and stolons during the growing 100
season.
80
from studies characterising this pathogen (Dobinson et al. 2000). 60
We have been able to correlate signal strength with numbers of
C. coccodes microsclerotia (Fig. 4a). Real-time PCR will be a 40
useful tool in developing effective management strategies for y = 14.541x + 15.249
V. dahliae and C. coccodes. Data obtained to date suggest that 20
R2 = 0.797
the number of potato crops planted in a field directly influences
0
the soil population of C. coccodes (Fig. 4b). As the number of 0 1 2 3 4 5 6
times potato is grown on a field increases, so does the population
of the black dot fungus. Fields with excessively high populations Number of potato crops
can be avoided and planted to a rotational crop. The rate of Fig. 4. Relationship of fluorescence (F1/F2) to microsclerotia of
metam sodium can be adjusted based on the level of V. dahliae Colletotrichum coccodes detected from artificially infested field soil (a)
in the soil optimising its use and minimising the overuse of this and the relationship between the number of potato crops and population
agrochemical. of C. coccodes in fields (n = 45) tested using real-time PCR (b).
VCGs are known to exist for both V. dahliae and C. coccodes
and represent a significant amount of diversity among
populations of these two pathogens (Joaquim and Rowe 1991; in the field, before harvest, our studies have demonstrated that
Strausbaugh 1993; Heilmann et al. 2006; Nitzan et al. 2006a). high infection rates in storage are usually due to postharvest
Similar to V. dahliae, differences exist in aggressiveness among infections (Salas et al. 2000) and that the degree of wounding
VCGs of C. coccodes, and we are able to differentiate among and tuber pulp temperatures have a significant influence on
these groups using amplified fragment length polymorphism the development of this phase of the disease. Tuber pulp
(AFLP) analyses (Heilmann et al. 2006; Nitzan et al. 2006a). temperatures above 18◦ C increase postharvest infections by the
We believe AFLP analysis, once specific bands are converted pink rot pathogen (Salas et al. 2000). Therefore, an important
to sequence-characterised amplified regions or SCAR markers, cultural management practice for the water rot complex is to
will be a useful tool in further studies involving the biology and avoid harvesting potatoes when tuber pulp temperatures exceed
management of black dot (Heilmann et al. 2006). 18◦ C. Recently, a management tactic was developed to reduce
post-harvest infections of P. erythroseptica with the application
Pink rot and leak tuber rots of phosphoric acid onto tubers being placed into storage (Miller
The incidence and severity of pink rot and leak tuber rot can et al. 2006).
vary considerably from year to year. This variability necessitates Most potato cultivars in production in the USA are susceptible
vigilance by growers in the careful implementation of the to both pink rot and leak tuber rot (Salas et al. 2003), although a
management options that exist for each disease. For example, few cultivars have moderate levels of resistance to one, but not
tuber pulp temperatures at harvest are known to have a significant both, of these diseases. We have recently developed a source
impact on the development of leak tuber rot (Salas and Secor of resistance to both pink rot and leak tuber rot, resulting
2001). The incidence and severity of leak tuber rot is significantly from a somatic hybrid backcross clone derived from Solanum
higher at tuber temperatures above 21◦ C and is nearly arrested at berthaultii and S. etuberosum (Thompson et al. 2007). It will
temperatures below 10◦ C. Similar studies by our research group be some time before this source of resistance is reflected in
have determined that tuber pulp temperatures at harvest also commercially accepted potato cultivars.
influence pink rot development (Salas et al. 2000). Although Since most potato cultivars are susceptible to pink rot and
infection by P. erythroseptica was initially believed to occur only leak tuber rot, the industry has developed a reliance on theManagement of soilborne diseases of potato Australasian Plant Pathology 113 fungicide mefenoxam for disease management. Mefenoxam Dakota, Wisconsin and Michigan. Based on data generated by provides excellent control of pink rot, and fair control of our research group, the inheritance of mefenoxam resistance leak tuber rot when applied in furrow (Taylor et al. 2004). in P. erythroseptica, a homothallic fungus, appears to be The advantage of at planting applications of mefenoxam, in inherited quantitatively (Abu El Samen et al. 2005). Populations furrow, compared with foliar applications for pink rot control, of the pathogen become qualitatively less sensitive to the has also been demonstrated in Australia (Wicks et al. 2000). fungicide in successive generations indicating that once shifts The difference in the level of disease control of pink rot in sensitivity occur, they are not reversible. Most recently, we relative to leak tuber rot is directly related to differences in have demonstrated that mefenoxam resistant populations of aetiology between the two diseases (Taylor et al. 2004). After P. erythroseptica are not only parasitically fit, but in the presence the application of mefenoxam to potato plants, it is known to of the fungicide they are likely to cause more disease than in concentrate in the periderm of tubers (Bruin et al. 1982), a the absence of the fungicide (Taylor et al. 2006). These results phenomenon made possible only with phenylamide fungicides have a significant impact on disease management strategies and since they are symplastically mobile in plants and capable of demonstrate the impact that over reliance on a single tactic movement in the phloem. Wounds made at harvest breech the can have on an industry. As a result, we continually monitor barrier to infection afforded by mefenoxam, thereby reducing the P. erythroseptica populations on individual farms and once efficacy in leak tuber rot control relative to pink rot (Taylor et al. mefenoxam resistance is detected, we recommend this fungicide 2004), since P. ultimum is a strict wound pathogen. The level no longer be used. Phosphorous acid based fungicides apparently of control of leak tuber rot which is provided by mefenoxam provide suppression of pink rot, but have no effect on leak is not economic, therefore, we recommend potato growers do tuber rot (Johnson et al. 2004). Unfortunately, the multiple not use this fungicide solely for this purpose. In other words, in applications of phosphorous acid required to achieve this level the absence of disease pressure from pink rot, growers should of control is very expensive, ∼2–3 times the cost of mefenoxam avoid using mefenoxam for the control of leak tuber rot. It is based fungicides and may not be economical. important to note, however, that wounding of tubers at harvest When lacking host resistance and chemical control, potato can also negate the effects of mefenoxam application with the producers are left to manage pink rot and leak tuber rot pink rot pathogen (Fig. 5). Therefore, cultural practices that using cultural methods that limit wounding and encourage encourage skin set and minimise wounds at harvest are important tuber maturation. They should also harvest when tuber pulp in preserving the level of control afforded by the application of temperatures are
114 Australasian Plant Pathology N. C. Gudmestad et al.
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